Thursday, March 29, 2012

I have always found it difficult to start writing, about anything. The first paragraph is always the one that puts everything in context, so it is extremely important to write it in a way that the reader feels attracted and continues reading. So if I’m going to write about Trinidadian guppies and their ectoparasites, I guess I should start by talking about parasites and why they’re such amazing study systems to answer a variety of evolutionary and ecological questions. Okay, here we go. Fact #1: parasites are the most common life form, with up to 75% of species in a food web consisting of parasites. Fact #2: Parasite-related pathology (damage) results in the activation of the energetically costly host immune response. The resources that are used to fight the infection, then, are not available for reproduction or growth. Fact #3: Infected individuals are not sexy, which can be rephrased as: infected individuals have lower fitness. The idea here is that individuals (particularly males) that have few or no parasites probably have a strong immune system (good genes). So if they don’t have to waste energy in strong immune responses, what will they devote it to? Yes, reproduction and growth. Females will then prefer these particular males because their offspring will be also big, good at fighting parasites and, eventually, at accessing mates. Sometimes, however, these traits that increase fitness in regards to parasitism may be disadvantageous for other sources of selection. Here is where everything gets complicated, but also much more interesting.

For this study, we were particularly interested in how two sources of selection interact in nature: parasitism and predation, a very well studied selective force. The best approach to answer this question is to use a model organism for which there is a good understanding of its response, both ecological and evolutionary, to predation. And so we chose the Trinidadian guppy (see picture below). Evolutionary biologists are very familiar with guppies because they’ve been studied for over 30 years in their natural environment, but probably for somebody unrelated to this field guppies are just a fish that you can buy in a pet shop. Guppies are sexually dimorphic live-bearing fish endemic to South America and adjacent islands. Due to their very short generation time, guppies have shown very fast adaptation to a variety of environments. Many of these environments can be classified by their mortality rates due to predation, and have thus been classically cataloged as high- or low-predation. Guppy populations that inhabit these two distinct environments have diverged in their life histories, behavior, and ecology in general (i.e. guppies have evolved different adaptations to their particular predation environments). For example, guppies that have evolved under high predation pressure show early sexual maturation and increased reproductive effort (how much of their body weight is made of embryos). They also tend to have many embryos, but small ones. In addition, guppies also differ in their schooling and mating behaviors. Males from low-predation environments engage females in courtship and pursue them, displaying their coloration – males with more coloration tend to have higher reception from females. In contrast, in high-predation environments males tend to approach females quickly, because courtship behavior increases the chances of being spotted by a predator. Finally, when fish from a high-predation population are introduced to a previously guppy- and predator-free environment, they evolve to trait values similar to those of natural low-predation fish.

If guppies have adapted to predation, how could this affect their adaptations to parasitism? I mentioned earlier that parasite-related pathology is energetically costly, not only because the immune system is activated, but also because of physical damage. The host becomes lethargic – just remember the last time you had a cold, or even better when you traveled to that beautiful tropical country and tried the delicious street food, and you’ll know what I mean. Natural selection should favor immunologically strong guppies in high-predation environments, because infected fish are easier prey. Basically, genes for weak immune systems are being constantly removed from the population by the predators.

Although there may be many other ways in which predation and parasitism interact in the Trinidadian guppy system, this simplified view had empirical support. Joanne Cable and Cock van Oosterhout (2003) compared resistance to a ubiquitous ectoparasite between a high- and a low-predation guppy population from the Aripo. They found that, in the lab, fish from the high-predation environment were much better at limiting their parasite load, and on average the length of their infections was much shorter than for low-predation guppies. Moreover, a later study by the same authors found that in the lab, when infected with the same ectoparasite, larger guppies had higher parasite loads and also higher mortality rates (Cable and van Oosterhout, 2007). In wild populations, then, guppies could be under strong parasite selection for earlier maturation (life-history theory predicts that when there is increased mortality in larger or older fish, earlier maturation should be favored by selection). Therefore, adapting to predation should also be beneficial for parasitism, and hence high-predation guppies are more resistant to parasites. However, the previous studies were based on only one river, the Aripo. In order to make generalizations of this pattern across the different rivers in Trinidad a larger number of rivers would need to be compared.

To test whether high-predation guppies are better adapted to parasitism than their low-predation counterparts, we compared guppy phenotypic response to the ectoparasite Gyrodactylus in traits such as body growth, reproductive effort, number of embryos, and infection dynamics for fish from eight populations (4 high- and 4 low-predation), from four rivers: Aripo, Marianne, El Cedro, and Quare. The phenotypic response was compared between the populations exposed to parasites, but also with control populations that were kept parasite-free. We conducted our experiments in mesocosms or artificial stream channels that closely replicate the natural conditions that guppies experience in the wild, using Gyrodactylus from each guppy population (photo below). This allowed us to make inferences about infection dynamics and phenotypic response in nature. (I would like to use this opportunity to thank David Reznick from UC Riverside and the FIBR Project: From Genes to Ecosystems for facilitating the use of these mesocosms).

Using Gyrodactylus has many advantages. They commonly infect high- and low-predation populations, and in the lab they induce up to 50% mortality in guppies. They are specialist parasites with extreme progenesis: each mature female has in its uterus a fully developed embryo, which in turn has a developing embryo. This allows them to have exponential population growth rates and strong demographic effects on the host population, even in periods of time as short as 27 days, which was the duration of our experiment.

Our results were not consistent with previous work with fish from the Aripo river. We found great variability in infection dynamics and phenotypic response between rivers. However, guppies that were exposed to parasites, regardless of the predation environment, consistently had lower body growth and higher reproductive effort than those in the control channels. This was coherent with previous theory and empirical work.

There are a couple of possible explanations about the drivers of these patterns. First, infected individuals may have to re-allocate energy to immune response to fight the infection, leaving less energy for growth. Second, Gyrodactylus pathology may be severe, so infected individuals eat and grow less. Although both are possible, it seems that the former is a more plausible explanation. The infection levels we observed in our experiments are lower than what is observed in the lab, but consistent with what we see in nature. In addition, we did not detect any effect of parasite load (number of parasites) on body growth or reproductive effort, meaning that it was the exposure to parasites, and not the actual infection, that was inducing these responses. Reduced body growth has another adaptive value: since larger fish tend to have more parasites and higher mortality rates, a smaller body size could reduce the high costs of Gyrodactylus infections.

In conclusion, our study reveals that guppy phenotypic response to Gyrodactylus infection is similar across populations from both high- and low-predation environments, although the degree and the strength of this response is quite variable across the different rivers. However, there was no consistent pattern when comparing infection dynamics, and an important final point should be made here. We used parasites that have a coevolutionary history with their respective guppy population. Coevolution between parasites and their host is temporally and spatially dynamic, which could lead to divergent evolution of guppy resistance and parasite virulence. Therefore, our results could be the artifact of coevolution, rather than the interaction of predation and parasitism, making inferences somehow difficult. But don’t worry; we are already working on this…

Cable, J. & van Oosterhout, C. 2007. The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. International Journal for Parasitology37, 1449-58

Monday, March 12, 2012

Day 4 was a diving day, with manta rays, garden eels, and hammerhead sharks to distract me from eco-evolutionary musings. But on day 5 it was back to work; this time in the wet highlands (picture below) rather than the dry(ish) lowlands. Our goal in sampling these multiple sites is to examine morphological variation in finches across different habitats in order to gain further insight into the ecological forces driving evolutionary diversification. The highlands are simultaneously invigorating and depressing. Invigorating because they are lush and wet – like a miniature rainforest – depressing because so little habitat is left and much of it is over run by invasive species. The most dramatic of these is the yummy blackberry, which carpets the ground below the trees. It is so stressful to the park service that their solution for control is simply spray to roundup. This kills the blackberries plenty dead but it also kills all the native plants. Go figure.

Invasive species are known to be the drivers of contemporary (rapid) evolution the world over, so why should it be any different in Galapagos? This famous crucible of evolution is presumably still crucibiling - perhaps more so now that invasive species are becoming so widespread. For instance, Darwin’s finches are famous for evolving rapidly in response to changing environmental conditions: larger beaks evolve when small seeds are depleted during droughts – but larger beaks evolve during droughts when a larger beaked competitor depletes the larger seeds. Remarkably, it seems that a major player in this evolution might be an invasive plant. By “might” I mean that the major player is known – a very large/hard seed of the plant Tribulus cistoides – but it might or might not be invasive depending on who you talk to. Perhaps one of best examples of evolution in action in nature is actually driven by an invasive plant species.

Now it seems that Darwin’s finches are experienced a dramatic new selective pressure – parasitism. Sometime in the past few decades the fly Philornis downsi invaded Galapagos and began to parasite the nestlings of native Galapagos birds, including at least 11 finch species. The adult flies are not parasitic but their spawn are – they creep out of the nesting material at night to suck the blood and juices of the nestlings. The earliest stages (instars) of this parasite even live inside the nostrils of the poor little finch babies. Now this sounds nasty enough but it looks even nastier. If you pick apart the nests of finches, you find large numbers of big fat juicy grubs in the nesting material (picture below) and the nestlings themselves show rather large and hideous holes in them from the nocturnal activities of their unwelcome nest mates.Adding injury to insult, these blood sucking maggots seem to have a huge impact on nestling survival and therefore the reproductive success of finches – as shown by a number of researchers (see citations below). For instance, some studies show very high failure rates of infected nests – and infected nests are very common. If infections levels are experimentally reduced, fledging success goes up. Given that these parasites seem to be wide spread on the islands, great concern has been raised regarding the possible negative impacts on finch populations. So why, then, do finches seem to be as abundant as ever. And why, in some years, do we catch lots of fledglings? How can we reconcile very high nest failure with demonstrable evidence of nesting success? One hypothesis is that the timing of parasitism is tied to the first clutch of finches, which then fails, but not the second clutch, which then succeeds. Another hypothesis is that some (unknown) areas of low parasitism are providing a pool of finch immigrants that are keeping populations high even in areas of severe nesting failure. Or maybe we have yet to see major impacts simply because finches are very long lived and, when the adults produced before the current major infestations die of old age or other insults, the populations will start to decline. My own hypothesis is that fledging success may not be the limiting factor in Darwin’s finch population size – perhaps it is instead food resources for adults during dry periods. If so, a decline in the number of fledglings owing to parasitism won’t cause the population to decline.

What remains indisputable is that these darn maggots do kill lots of fledglings, so selection would presumably favor the evolution of adaptive responses by the finches. Some work has shown that finches do show acquired immunity, meaning that exposure to parasites increases subsequent resistance to (or tolerance of) parasites, but whether or not this or other forms of resistance/tolerance are evolving is not certain. This seems to me a great place to look for eco-evolutionary dynamics. That is, one could test whether resistance or tolerance were evolving and then assess the impact of this evolution of finch population dynamics. This is not for me, however, as it would require studying nocturnal maggots that suck the blood of cute little nestings.

Sadly, this is the end of my short but productive trip to Galapagos. I am now sitting in the Guayaquil Airport waiting for thundershowers to clear in hopes of catching the red eye to Miami.

Thursday, March 8, 2012

One of the things that Darwin found so striking about the Galapagos was the tameness of the fauna. He tells many stories about how various animals simply had no fear of humans. A small boy sat beside some water and hit finches with a stick until he had his dinner. Darwin caught a marine iguana and threw it into the ocean and it swam right back to him to be thrown in again – and again – and again. Not to mention the hawks that perched on a person’s head, tortoises you can ride on, and so forth. Darwin attributed this innocence to the lack of prior experience of Galapagos fauna with humans – as opposed to mainland fauna that won’t let humans anywhere near them. In his Voyage of the Beagle, he wasn’t very explicit about why this difference might have arisen – that is, he didn’t provide a formal evolutionary explanation. But that is, clearly, the reason. Animals that live with humans evolve to be afraid of them because genes for being afraid confer life and are thereby passed onto the next generation. Of course, animals can also learn to avoid humans but this learning ability is still often an evolutionary response to human depredation.

Galapagos fauna are still very tame despite now having several centuries of evolutionary experience with humans. You can still walk within several feet of a finch or iguana or tortoise, although hitting them with sticks or throwing them in the water or riding on them is certainly no longer a common activity. So it seems that Galapagos fauna have not evolved to avoid humans despite being persecuted by humans on the Galapagos for centuries. Or have they? Perhaps they have evolved and our perceptions are subject to something like the “shifting baseline” phenomenon. The shifting baseline refers to the fact that we tend to think the state of the recent past is what is normal – when it might be anything but. Thus, we might think that we should recover our fish stocks to levels seen in the 1950s (or whenever) because we think those were the “right” levels based on our past experience when, really, they were much higher even earlier. In essence, our baseline for what is “normal” gets reset each generation by our own experiences. In the case of Galapagos tameness, maybe the baseline (what we are used to for tameness based on our experience with mainland fauna) isn’t shifting, and maybe the Galapagos fauna are getting less tame, but maybe they are still so much more tame than the baseline that we don’t notice. I suppose we could call it the “distant baseline” phenomenon.

So how would one escape from this baseline constraint? One possibility might be to compare Galapagos fauna at places that have more or less human activity. In my first few years at Galapagos, I tried very hard to get pictures of Sally Lightfoot Crabs, those beautiful red crabs that dot the lava along the ocean as they pick away at the algae on the rocks. But at the site I was staying, beside the town of Puerto Ayora, it was really hard. Whenever I got close, they would leap away to a new rock or scuttle under it. I never got a good photo – although I was really impressed by their agility. A few years later, I started doing work at Borrero Bay, a site on the north side of the island away from any human influence. All of a sudden these crabs were everywhere and I could just walk right up to them. I soon had hundreds of photos with a crab almost filling the frame (above). I would often have to back up because my telephoto lens wouldn’t focus close enough.

This difference in crab behavior between a site with lots of humans (Puerto Ayora) and a site without humans (Borrero Bay) got me to thinking that perhaps the crabs at the former have indeed evolved to be scaredy cats. My initial thought was that dogs chased and killed them but I am also now told that humans hunt and eat them or use them for bait – or at least they used to. How has this difference arisen? Has there been genetic divergence in behavior between the two sides of the island? This might be surprising as these crab larvae are presumably pelagic and so might expect to be a single mixed population on that scale. Or are we now seeing the activation of learning behavior that has evolved elsewhere in these crabs and been retained following their colonization of Galapagos? Anyway, this was the state of my thinking until yesterday. Yesterday I took a walk out on beach by Puerto Ayora and the crabs were still very shy. But this time, I noticed several small lava heron stalking them (above), and dashing out in an effort to catch them – I didn’t see any successes. Could it be that herons are more common here than at Borrero and have driven the divergence in behavior? Or could it be that herons have caused the evolution of learning to avoid two-legged things on the beach in the Galapagos in general, and this is simply then turned on at Puerto Ayora owing to the commonness of humans. The other observation was that the crabs were, in fact, very tame (below) at a small site on the grounds of the Charles Darwin Research Station beside Puerto Ayora (although not nearly as tame as at Borrero). Non-station people are not allowed at this site and crab persecution is presumably very low – but the herons are present. So maybe this supports the human effect hypothesis. But at the same time, it suggests that the effect must be due to learning (evolved though it might be) rather than genetic differences between sites – as the differences were on a very small scale.So what will happen in the future? If the changes are caused by humans, then I would expect the tameness to come back – since humans are no longer allowed to kill native Galapagos critters. Maybe we are starting to see this at the research station. Anyway, it is a cool problem that I hope someone looks at some day.

More:1. The shifting baseline: http://en.wikipedia.org/wiki/Shifting_baseline2. An example of human effects on tameness from a study of reef fish conducted by Kiyoko Gotanda, now a PhD student in the Hendry lab: http://www.springerlink.com/content/a541271237060604/

Tuesday, March 6, 2012

Yesterday I arrived in Galapagos for a short trip to touch bases with our field crew (“Team Pinzones”) working on the evolution of Darwin’s finches and the effects they have on the plant community. Flying in, it was immediately clear that things were different from most other years I have been here. Even Isla Baltra, the usually bone-dry island where the airplane lands, was covered with green. And I saw several large pools of water while driving from the airport to the ferry that takes one across the channel between Baltra and the main island of Santa Cruz. The rainy season was really here! I made it to the Charles Darwin Research Station without serious mishap, which was actually somewhat miraculous as my taxi driver was so sleepy he had his eyes closed more than half the time. I tried to keep him awake through conversation but I very quickly exhausted my Spanish vocabulary. I would therefore wait a few minutes and ask the same questions again – which worked fine since he was too sleepy to remember what I had said five minutes previously.

The first afternoon, we (Luis Fernando De Leon, Joost Raeymaekers, Jeff Podos, and myself) went into the “field” beside the research station. It is too hot to catch finches during the middle of the day (for us and them) and so we headed out about 4 pm. Our goal in general is to use mist nets to catch as many finches as possible to find out which of our previously tagged birds are still alive and to also tag more birds to follow over next year. As the finches are caught, they are removed from the net and brought to our banding “station.” The finches are usually quite mad when they are caught (see photo below) and seem to take great pleasure in biting every finger that comes within beak length. And man, can they bite hard. At the banding station, they are measured, photographed, banded, blood-sampled for DNA, and released. These procedures allow us to estimate selection acting on traits such as beak size and shape, and to estimate gene flow and interbreeding within and between species. As always at Academy Bay, the catching was quite good. What was different from past years was the verdure. It was quite simply green everywhere: green on the ground, green in all of the trees, green over all the boulders and rock walls. The only breaks in the green were wonderful yellow and white flowers that I haven’t seen in abundance since 2002, when my visit last coincided with a really wet period.

The next morning, we went to El Garrapatero, our main research site. This involves getting up at 4:30 am and having a taxi pick us up at 5:00 am for the 40 minute or so drive to El Garrapatero. We then all pile out of the truck and head off into the bush to set up mist nets in places where we think that the finches will soon be flying by. We then collect data from the captured birds as described above and for the same purpose: to estimate selection and gene flow. This information is particularly useful for El Garrapatero because one species found there (Geospiza fortis) has a beak size distribution that is bimodal: small and large morphs are present with relatively few intermediates. By contrast, the G. fortis population at Academy Bay was historically bimodal but is now only unimodal: perhaps owing to human activities that have altered the selective forces that normally promote bimodality. Luis recently wrote a blog post about the paper he just published on this topic: http://ecoevoevoeco.blogspot.com/2011/10/homo-sapiens-influence-micro.html.

I have spent many hours walking around at El Garrapatero in past years when it was dry, and so it was interesting to now do the same under very wet conditions. In addition to the greatly increased amount of vegetation (see the photo above) – so much so as to make it hard to find some of the trails of previous years – what struck me the most was the increase in insects. Yellow, blue, and black butterflies flit everywhere, huge Galapagos carpenter bees are constantly buzzing over the ground and in the bushes, hoverflies are holding their position in midair, countless spiders of various sizes and shapes are suspended between each pair of shrubs and therefore soon on our pants and shirts and hats (a huge one leaped out when I opened my backpack when we got back to the station), and caterpillars everywhere: on plants large and small, in the webs of very happy spiders (see photo below), in the beaks of finches, everywhere. This exuberance of animal life surpasses any that I have previously seen during my visits and it seems to really drive the entire system. It is almost like everything goes into suspended animation between rain events and then everything wakes up and immediately explodes into frenetic activity. In fact, it isn’t almost like that – it is like that.